Genetics account for a only small portion of differences in the physical traits of organisms, which has led evolutionary biologists to wonder about the role the environment and other factors might play in species divergence.

The report in the journal Proceedings of the Royal Society B clarifies this relationship, for the African cichlid fish.

Led by University of Massachusetts-Amherst geneticist Craig Albertson, the study explores how a “bizarre behavior” that is part of the cichlids’ early larval developmental environment influences changes in their craniofacial, or skull and face, bones.

The team studied a “vigorous gaping” behavior in larval cichlids, in which they open and close their mouths rapidly. This behavior begins shortly after the cartilaginous lower jaw forms, and before bone deposition begins.

“We predicted that the baby fish are exercising their jaw muscles, which should impose forces on the bones they attach to, forces that might stimulate bone formation,” Albertson said.

The team found that gaping frequency varied by species, reaching as high as 200 per minute. The gaping frequencies varied “in a way that foreshadows differences in bone deposition around processes critical for the action of jaw opening,” the authors wrote.

“For over 100 years, we’ve been taught that the ability of a system to evolve depends largely on the amount of genetic variation that exists for a trait,” Albertson said. “What is ignored, or not noted for most traits, is that less than 50 percent of genetic variation can typically be accounted for by genetics.”

Albertson said that while variations in skull shape are largely heritable, scientists can find genetic variability for only a small portion of differences in bone development.

“In my lab, we have shifted from elaborating our genetic models to looking more closely at the interaction between genetics and the environment,” Albertson said.

The relationship between environmental influences and species development is known as epigenetics. The term was coined in the 1940s and included anything not encoded in the nucleic acid sequence – a series of letters that signify the order of nucleotides in a DNA molecule. While epigenetics has since come to refer to how the 3D structure of the DNA molecule is modified, the team operated under the original definition.

In this sense, gaping is an aspect of a dynamic developmental environment, according to Albertson.

“Bones are not forming in static lumps of tissue. Rather, they are developing as part of, and perhaps in response to, a highly complex and dynamic system,” he said.

Since species differ in gaping rate, the team decided to test the theory that variations in bone development could be accounted for by differences in this behavior.

“We performed experiments to see if we could slow the rate in fast-gaping species and speed it up in slow-gaping species, and to see if this behavioral manipulation could influence bone development in predictable ways,” Albertson said.

The difference in skeletal morphology — alterations in the skeleton in response to genetic adjustments — fostered by simple changes in behavior was similar to what was predicted to be caused by genetic factors.

“What I find really exciting is that in 15 years of manipulating the genetics of craniofacial bone development we can account for up to 20 percent of the variability, so it’s modest,” Albertson said. “When we manipulate gaping behavior, we can influence developmental variability by about 15 percent, which is comparable, almost equal, to the genetic response.

“When I give talks, this is what surprises colleagues the most, that the environmental effect is on par with the genetic effect, and that it is not systemic but highly specific to important bones involved in fish feeding.”

Albertson said this behavior is not surprising given that nature promotes efficiency. Adjusting an adaptive response to a specific niche improves the likelihood of survival.

“This is just the beginning. Our field has been entrenched in a gene-centered view of evolution for nearly a century,” Albertson said. “My hope is that this study adds to a growing body of literature that shows there are other important sources of variation.”

Albertson said that the next step is to determine how environmental stimuli influence development.

“We now need to understand how bone cells sense and respond to their mechanical environment,” he said. “What are the molecules that enable this mechano-sensing?”

(Photo of the jaw of a larval cichlid courtesy of the University of Massachusetts at Amherst.)